Nontriplet feature of genetic code in Euplotes ciliates is a result of neutral evolution
Sofya A. Gaydukova, Mikhail A. Moldovan, Adriana Vallesi, and Pavel V. Baranov Authors Info & Affiliations
Edited by Eugene Koonin, NIH, Bethesda, MD; received December 21, 2022; accepted April 12, 2023
May 22, 2023
120 (22) e2221683120
https://doi.org/10.1073/pnas.2221683120
Significance
In this work, we provide compelling evidence that Euplotes genetic code violates the triplet nature of the genetic decoding that was thought to be universal. Thus, Euplotes possess the most extreme example of genetic code variation described so far. The nontriplecy arises from abundant ribosomal frameshift sites with no regulatory function, where stop-codons distant from the 3′ transcript end specify +1 or +2 ribosomal frameshifting with high accuracy. We show that this violation of the triplet coding in Euplotes is brought about and further maintained by neutral evolution rather than selective processes but still is irreversible.
Abstract
The triplet nature of the genetic code is considered a universal feature of known organisms. However, frequent stop codons at internal mRNA positions in Euplotes ciliates ultimately specify ribosomal frameshifting by one or two nucleotides depending on the context, thus posing a nontriplet feature of the genetic code of these organisms. Here, we sequenced transcriptomes of eight Euplotes species and assessed evolutionary patterns arising at frameshift sites. We show that frameshift sites are currently accumulating more rapidly by genetic drift than they are removed by weak selection. The time needed to reach the mutational equilibrium is several times longer than the age of Euplotes and is expected to occur after a several-fold increase in the frequency of frameshift sites. This suggests that Euplotes are at an early stage of the spread of frameshifting in expression of their genome. In addition, we find the net fitness burden of frameshift sites to be noncritical for the survival of Euplotes. Our results suggest that fundamental genome-wide changes such as a violation of the triplet character of genetic code can be introduced and maintained solely by neutral evolution.
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